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Simultaneous Hyperaccumulation of Nickel and Cobalt in the Tree Glochidion Cf

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Simultaneous Hyperaccumulation of Nickel and Cobalt in the Tree Glochidion Cf www.nature.com/scientificreports OPEN Simultaneous hyperaccumulation of nickel and cobalt in the tree Glochidion cf. sericeum Received: 9 October 2017 Accepted: 25 April 2018 (Phyllanthaceae): elemental Published: xx xx xxxx distribution and chemical speciation Antony van der Ent1,2, Rachel Mak3, Martin D. de Jonge 4 & Hugh H. Harris5 Hyperaccumulation is generally highly specifc for a single element, for example nickel (Ni). The recently-discovered hyperaccumulator Glochidion cf. sericeum (Phyllanthaceae) from Malaysia is unusual in that it simultaneously accumulates nickel and cobalt (Co) with up to 1500 μg g−1 foliar of both elements. We set out to determine whether distribution and associated ligands for Ni and Co complexation difer in this species. We postulated that Co hyperaccumulation coincides with Ni hyperaccumulation operating on similar physiological pathways. However, the ostensibly lower tolerance for Co at the cellular level results in the exudation of Co on the leaf surface in the form of lesions. The formation of such lesions is akin to phytotoxicity responses described for manganese (Mn). Hence, in contrast to Ni, which is stored principally inside the foliar epidermal cells, the accumulation response to Co consists of an extracellular mechanism. The chemical speciation of Ni and Co, in terms of the coordinating ligands involved and principal oxidation state, is similar and associated with carboxylic acids (citrate for Ni and tartrate or malate for Co) and the hydrated metal ion. Some oxidation to Co3+, presumably on the surface of leaves after exudation, was observed. Hyperaccumulators are rare plants that accumulate metal and metalloid elements to extraordinarily high con- centrations in their living biomass that may be hundreds or thousands of times greater than is normal for most plants1–3. Hyperaccumulator plants can achieve such extreme levels of foliar sequestration due to enhanced uptake and translocation mechanisms4,5. Te hyperaccumulation phenomenon is extremely rare (exhibited by <0.2% of angiosperms) with ~70% of the 700 known hyperaccumulator species recorded for Ni1,6,7. Hyperaccumulator plants are found on all continents except Antarctica, in temperate and tropical biomes, with the greatest numbers found in New Caledonia, Cuba and the Mediterranean Region2,8–10. Te Ni concentrations that hyperaccumulator plants can attain in their leaves and transport fuids can be extreme. For example, two species from Malaysia can accumulate up to 2.4 Wt% Ni in the leaves (Psychotria sarmentosa – Rubiaceae) and up to 16.9 Wt% Ni in the phloem sap (Phyllanthus balgooyi – Phyllanthaceae) respectively11,12. Hyperaccumulation is not just an interesting biological phenomenon, but holds much promise for evolu- tionary, genetic and ecophysiological research, and, at the more ambitious end of benefcial use, the potential utilization in phytomining13. Nickel phytomining (also termed ‘agromining’) is a special type of farming of hyper- accumulator plants on ultramafc soils, followed by harvesting and incineration of the biomass to produce a high-grade ‘bio-ore’ from which Ni metal or pure salts can be recovered13. Te criteria for the selection of ‘metal crops’ include high biomass yield combined with high Ni concentrations in the above-ground biomass. Although substantial unrealized opportunities exist in tropical regions for Ni agromining14, appropriate agronomic sys- tems have not been developed to date15. In temperate and Mediterranean climate regions, phytomining trials 1Centre for Mined Land Rehabilitation, Sustainable Minerals Institute, The University of Queensland, St Lucia QLD, Australia. 2Laboratoire Sols et Environnement, Université de Lorraine, Nancy, France. 3Department of Chemistry, University of Sydney, Camperdown, Australia. 4Australian Synchrotron, ANSTO, Clayton VIC, Australia. 5Department of Chemistry, The University of Adelaide, Adelaide, Australia. Correspondence and requests for materials should be addressed to A.v.d.E. (email: [email protected]) or H.H.H. (email: [email protected]) SCIENTIFIC REPORTS | (2018) 8:9683 | DOI:10.1038/s41598-018-26891-7 1 www.nature.com/scientificreports/ using Alyssum spp. (Brassicaceae) have yielded >100 kg Ni ha−1 per harvest16. Considering a nickel price of USD $15 kg−1 (average 2010–2016 London Metal Exchange value of Ni) and a potential yield of ≥100 kg Ni ha yr−1, the economic potential of implemented Ni phytomining technology is substantial. Te commercial returns from phy- tomining, however, will be fnite due to the diminishing concentrations of the target metal in the substrate, but the time scale for economic phytomining may be considerable, estimated at 30 years at least13. Cobalt phytomining is potentially more proftable because of its higher value compared to Ni (Ni is $13 kg−1 and Co USD $94 kg−1 in March 2018), but foliar Co accumulation is much lower than for Ni. Te highest foliar Co concentrations have been reported in Haumaniastrum robertii (Lamiaceae) from the Democratic Republic of Congo (D. R. Congo) with 1 Wt% or 0.7 Wt% Co in culture17. High foliar Co have also been reported in Rinorea javanica (Violaceae) with up to 670 μg g−1 in natural conditions18 and Alyssum troodii (Brassicaceae) with up to 2325 μg g−1 in spiked soils19. In total 32 Co hyperaccumulator plants are known globally, of which 16 are from the south-eastern D. R. Congo growing on highly Co-enriched soils (the so-called ‘Copper Hills’)20,21. Although Co is not essential for plants, Co is required by symbiotic rhizobia of leguminous plants and free-living nitrogen-fxing bacteria22, while Ni is part of the enzyme urease23. Te toxicity of Ni and Co to plants is linked to oxidative stress, inhibition of photosynthesis, and Fe defciency resulting in retardation and inhibition of growth and chlorosis and necrosis of leaves24–27. Hyperaccumulation of Co was frst defned as >1000 μg g−1 foliar Co28, but later revised downwards to >300 μg g−1 2,3. Hyperaccumulation essentially consists of two discrete stages, abnormal uptake in the root with enhanced translocation, followed by efective tissue and cell-level seques- tration. Nickel hyperaccumulator plants achieve extraordinary levels of specifcity for Ni over other transition group elements, such as iron (Fe), Mn and Co as a result of yet unidentifed Ni-specifc membrane-transporters. Knowledge of the uptake, biotransformation and distribution of Ni in hyperaccumulator plants is critical in understanding the process of metal acquisition and metal tolerance29. Most chemical speciation studies on hyper- accumulator plants have reported results from bulk measurements, and therefore could not distinguish between the diferent compartments across the biopathways, including root, xylem, phloem, and leaves30. X-ray absorption spectroscopy (XAS) has been used to study Ni chemical speciation in Alyssum, Leptoplax and Noccaea hyperaccu- mulators and mixtures of citrate and malate ligation were reported, which were found to vary in diferent parts of the plants31,32. Limited research to date has applied synchrotron radiation study to tropical Ni hyperaccumulator plants and very little is known about the transformation of Ni species from uptake to storage in plant leaves. Co-localization of multiple elements is suggestive of a common transport system, whereas diferential accumu- lation patterns are suggestive of separate transporter pathways. Recent investigations on the distribution and chemical speciation of Ni in three diferent hyperaccumulator species from Sabah revealed that Ni is present in the form of Ni:citrate and preferentially accumulated in the epidermis and in the spongy mesophyll in the leaves and in the phloem in the roots and branches33. Te recently discovered Glochidion cf. sericeum (Phyllanthaceae) from Malaysia is unusual in simultaneously hyperaccumulating Ni and Co to approximately 1500 μg g−1 in the leaves, i.e. a ratio of ~1:1 Ni:Co11. Compared to most other Ni hyperaccumulator plants, with a mean Ni:Co of 475 for 24 diferent species34, this response, and the very high foliar Co concentrations it attains, is remarkable. Te current study used synchrotron X-ray fuores- cence microscopy (XFM) and XAS to investigate whether the distribution and associated ligands for Ni and Co complexation difer in Glochidion cf. sericeum. We aimed to determine the chemical speciation in frozen hydrated samples of diferent plant organs, tissues and transport liquid (xylem and phloem) from the root to leaves to gain an understanding of the mechanisms of transport and storage in this species. Results Herbarium XRF survey and taxonomical status of the study species. Glochidion is a very speciose genus of trees and shrubs with 200–300 species occuring from India to South China, Southeast Asia, Malesia, Australia and the West Pacifc35. In total, 33 species have been enumerated from Borneo36. An Herbarium X-ray Fluorescence (XRF) scanning survey was undertaken at the Forest Research Centre (FRC) Herbarium on all holdings of Glochidion (totalling 643 specimens). Te XRF scanning revealed the existence of several Ni hyperac- cumulator species which have been previously reported11, and anomalously (>300 μg g−1 corrected XRF values) high Co values in two unidentifed Glochidion specimens with 307 μg g−1 and 681 μg g−1 Co respectively, and in a specimen of Glochidion elmeri which had 539 μg g−1 Co (Suppl. Table 1). Herbarium specimens of G. cf. sericeum (held at the Sabah Parks Herbarium) were also measured with XRF and Co reached up to 951 μg g−1 Co in 19 leaves from the three specimens measured. Subsequent bulk analysis with ICP-AES of fragments obtained from these herbarium specimens gave mean values of 1159 ± 217 μg g−1 for Co and 2037 ± 205 μg g−1 for Ni. Glochidion cf. sericeum is a phyllanthoid branching medium-sized tree (5–8 m-high with a stem up to 12 cm in diameter) that grows in the understory of lowland primary mixed Dipterocarp forest (Fig. 1). Tis taxon is presently known from only one locality (‘Serinsim’) in the Northern Part of Kinabalu Park in Sabah (Malaysia), and we have not been able to fnd any other occurrences of this taxon to date.
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